Convergent Selection on Juvenile Hormone Signaling Is Associated with the Evolution of Eusociality in Bees
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bioRxiv preprint doi: https://doi.org/10.1101/2021.04.14.439731; this version posted April 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Jones, Rubin, Dudchenko et al., 2021 – preprint version - bioRxiv Convergent selection on juvenile hormone signaling is associated with the evolution of eusociality in bees Beryl M. Jones1,2,*, Benjamin E.R. Rubin1,2,*, Olga Dudchenko3,4,*, Karen M. Kapheim5, Eli S. Wyman1,2, Brian G. St. Hilaire3, Weijie Liu1,2, Lance R. Parsons2, S. RaElle Jackson2, Katharine Goodwin2, Shawn M. Davidson2, Callum J. Kingwell6,7, Andrew E. Webb1,2, Mauricio Fernández Otárola8, Melanie Pham3, Arina D. Omer3, David Weisz3, Joshua Schraiber9,10, Fernando Villanea9,11, William T. Wcislo7, Robert J. Paxton12,13, Brendan G. Hunt14, Erez Lieberman Aiden3,4,15,16,ⱡ, Sarah D. Kocher1,2,ⱡ,§ *These authors contributed equally ⱡThese authors contributed equally §Corresponding Author: [email protected] 1Department of Ecology and Evolutionary Biology, Princeton University, USA 2Lewis-Sigler Institute for Integrative Genomics, Princeton University, USA 3The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, USA 4Center for Theoretical Biological Physics, Rice University, USA 5Department of Biology, Utah State University, USA 6Department of Neurobiology and Behavior, Cornell University, USA 7Smithsonian Tropical Research Institute, 0843-03092 Panama City, Republic of Panama 8Research Center for Biodiversity and Tropical Ecology (CIBET), School of Biology, University of Costa Rica, San José, Costa Rica 9Department of Biology, Temple University, USA 10Illumina Artificial Intelligence Laboratory, Illumina Inc, San Diego, CA, USA 11Department of Anthropology, University of Colorado Boulder, USA 12Institute of Biology, Martin-Luther University Halle-Wittenberg, Germany 13German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Germany 14Department of Entomology, University of Georgia, USA 15Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech, Pudong 201210, China 16Faculty of Science, UWA School of Agriculture and Environment, University of Western Australia, Perth WA 6009, Australia Abstract Life’s most dramatic innovations, from the emergence of self-replicating molecules to highly-integrated societies, often involve increases in biological complexity. Some groups traverse different levels of complexity, providing a framework to identify key factors shaping these evolutionary transitions. Halictid bees span the transition from individual to group reproduction, with repeated gains and losses of eusociality. We generated chromosome-length genome assemblies for 17 species and searched for genes that both experienced positive selection when eusociality arose and relaxed selection when eusociality was secondarily lost. Loci exhibiting these complementary evolutionary signatures are predicted to carry costs outweighed by their importance for traits in eusocial lineages. Strikingly, these loci included two proteins that bind and transport juvenile hormone (JH) – a key regulator of insect development and reproduction. Though changes in JH abundance are frequently associated with polymorphisms, the mechanisms coupling JH to novel phenotypes are not well understood. Our results suggest novel links between JH and eusociality arose in halictids by altering transport and availability of JH in a tissue-specific manner, including in the brain. Through genomic comparisons of species encompassing both the emergence and breakdown of eusociality, we provide insights into the mechanisms targeted by selection to shape a key evolutionary transition. Keywords: comparative genomics, convergent evolution, eusociality, behavior, bees, juvenile hormone Introduction solitary individuals that live and reproduce independently to eusocial Organisms situated at the inflection point of life’s major evolutionary nests where individuals cooperate to reproduce as a group, and even transitions provide a powerful framework to examine the factors shaping polymorphic species that produce both solitary and social nests. This the evolution of these traits1,2. Halictid bees (Hymenoptera: Halictidae) evolutionary replication enables a comparative approach to identify the offer a unique opportunity to study the evolution of eusociality – social core factors that shape the emergence and breakdown of eusociality and colonies with overlapping generations and a non-reproductive worker provides insights into the most costly aspects of social life. caste. Within the halictid bees, there have been two independent gains3 We searched for signatures of positive selection associated and a dozen losses4 of eusociality. As a result, closely related species with the convergent gains of eusociality as well signatures of relaxed within this group encompass a broad spectrum of social behavior, from selection when eusociality is lost. These complementary patterns 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.14.439731; this version posted April 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Jones, Rubin, Dudchenko et al., 2021 – preprint version - bioRxiv indicate that these loci are associated with costs or trade-offs underlying all with chromosome-length scaffolds (Fig. 1; Fig. S1). We selected the maintenance of social traits. We find that some of the targets of species with well-characterized social behaviors that encompass both selection implicated in the origins and elaborations of eusociality, such independent origins and six repeated losses of eusociality3 (Fig. 1a-b). as young, taxonomically restricted genes5 and gene regulatory elements6, Sampling closely-related eusocial and solitary species alongside known also show relaxation of selective pressures when social behavior is lost, non-eusocial outgroups provides a powerful framework to examine the and we uncovered four genes strongly associated with the evolution of molecular mechanisms shaping the evolution of social behavior in this eusociality in halictid bees, including the two primary juvenile hormone group1. binding proteins (JHBPs): apolipoprotein7–9 and hexamerin11010,11. Assemblies ranged in size from 267 to 470 Mb, with estimated These results, combined with our analysis of JH localization in insects, numbers of chromosomes ranging from 9 to 38 (Table S2). Broadly, we provide new insights into how JH signaling has likely been modified to find that, in contrast to mammalian species (Fig. S2), genomic shape the evolution of eusociality. rearrangements among the bee species occur disproportionately within rather than between chromosomes (see Fig. 1c, Fig. S3). Consequently, A new comparative genomic resource for studying the loci that are on the same chromosome in one bee species also tend to evolution of eusociality occur on the same chromosome in other bee species. This observation is similar to previous findings in dipteran genomes12,13 and may indicate a We generated comparative genomic resources for halictids consisting of broader trend during the evolution of insect chromosomes. 15 de novo genome assemblies and an update of 2 additional assemblies, To increase the quality of genome annotations, we generated Figure 1. Comparative genomic resources for halictid bees. (a) Halictid bees encompass a wide range of social behaviors, from solitary to eusocial. Solitary species (yellow) nest and reproduce independently. Reproductive queens from eusocial species (blue) initiate colonies with offspring that include non-reproducing workers. Individuals from polymorphic species (green) are capable of both solitary and eusocial reproduction. Non-eusocial outgroups (red) reproduce independently, and include both solitary (Nomia melanderi, Dufourea noveangliae) and communal (Agapostemon virescens) nesting species. (b) Within the Halictinae, there have been at least two independent gains of eusociality and over a dozen independent losses of eusociality. Colors at branch tips indicate the behavior of each species. Circle sizes are proportional to the total number of orthologs with evidence for positive selection on each terminal branch (abSREL tests in HyPhy16; FDR<0.1). Light blue rectangles denote the two independent gains of social behavior in this family; their width is proportional to the number of orthologs with evidence for positive selection on each origin branch. Proportions of complete, fragmented, and missing BUSCO orthologs are shown for each genome. (c) Genomic data aligned to the outgroup Nomia melanderi. The 14 N. melanderi chromosomes are represented as a circular ideogram with consecutive chromosomes shown in alternating dark and light gray. The area inside the ideogram comprises 18 color-coded circular tracks, each corresponding to one L. calceatum chromosome, and the y-axis of these circular tracks represents the frequency of regions that align to the corresponding region in the N. melanderi genome. Usually, most of the alignments fall into a single “wedge”, indicating that each L. calceatum chromosome corresponds to just one N. melanderi chromosome. The pattern is typical for the bees we studied (see Fig. S3). Outer blue line plot indicates the number of branches in the phylogeny where positive selection was detected at each gene (abSREL, p<0.05). The